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University of São Paulo

“Luiz de Queiroz” College of Agriculture

Free living astigmatid mites (Astigmatina): new taxa, rearing and use for

mesostigmatid (Mesostigmata) predatory mite production

Marina Ferraz de Camargo Barbosa

Thesis presented to obtain the degree of Doctor in Science. Area: Entomology

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Marina Ferraz de Camargo Barbosa B.S. and B.Ed. in Biology

Free living astigmatid mites (Astigmatina): new taxa, rearing and use for mesostigmatid (Mesostigmata) predatory mite production

versão revisada de acordo com a resolução CoPGr 6018 de 2011

Advisor:

Prof. Dr. GILBERTO JOSÉ DE MORAES

Thesis presented to obtain the degree of Doctor in Science. Area: Entomology

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Dados Internacionais de Catalogação na Publicação DIVISÃO DE BIBLIOTECA - DIBD/ESALQ/USP

Barbosa, Marina Ferraz de Camargo

Free living astigmatid mites (Astigmatina): new taxa, rearing and use for mesostigmatid (Mesostigmata) predatory mite production / Marina Ferraz de Camargo Barbosa. - - versão revisada de acordo com a resolução CoPGr 6018 de 2011. - - Piracicaba, 2016.

136 p. : il.

Tese (Doutorado) - - Escola Superior de Agricultura “Luiz de Queiroz”.

1. Astigmatina 2. Ácaros de alimentos armazenados 3. Ácaros associados a abelhas 4. Acaridae 5. Pyroglyphidae 6. Echimyopodidae 7. Criação massal 8. Laelapidae 9. Rhodacaridae I. Título

CDD 595.42 B238f

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To my husband

Marcelo Elias Delaneze

For his love and unbreakable support. You are the salt of the Earth.

To my parents

Anna Maria Perosa Ferraz de Camargo Divaldo Bandória Barbosa

For their support, and constant encouragement I have received over the years

Offer

To Dr. Gilberto José de Moraes

For setting an example of excellence as a researcher, mentor, instructor and role model

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ACKNOWLEDGEMENTS

My sincere thanks goes to Dr. Barry OConnor and Dr. Pavel Klimov who provided me an amazing opportunity to join their team for a year, in which they taught me about this amazing mite group, provided me access to the laboratory and research facilities. Without their precious support, it would not be possible to conduct this research;

I would like to express my deepest gratitude to Prof. Dr. Carlos H. W. Flechtmann, for assistance provided whenever needed and for all good talking over the years;

To Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo especially to

“Departamento de Entomologia e Acarologia”, for providing the necessary support for

developing this work;

To “Programa de Pós-Graduação em Entomologia”, especially to its coordinators, Dr. José Mauricio Simões Bento and Dr. Fernando Luis Cônsoli, and the secretary Andrea Varella Sintoni, for supporting my activities;

To the team of EEB, University of Michigan, for all the support provided since my first day at Ann Arbor;

I thank my fellow labmates, Ana C. Cavalcante, Daniel C. Oliveira, Diana M. Rueda, Érika P. J. Britto, Fernanda de C. N. Esteca, Geovanny Barroso, Grazielle F. Moreira, Jandir C. Santos, Letícia H. Azevedo, Marcela M. R. da Silva, Paula C. Lopes, Peterson R. Demite, Raphael C. Castilho and Renan V. da Silva for the help, stimulating discussions and for all the fun we had had in the last four years;

To Pamela Murillo and Juan Rojas for the friendship during our staying in A2;

To the scientific laboratory technician, Lásaro V. F. da Silva, for laboratory help and activities support;

I would like to thank the exemplary librarians of the “Biblioteca Central”, especially those

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To my dear friends Wiolene and Thais for all the laugh they provided;

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CONTENTS

RESUMO ... 9

ABSTRACT ... 11

1 INTRODUCTION ... 13

References ... 15

2 A NEW SPECIES OF Thyreophagus (ACARI: ACARIDAE) FROM BRAZIL, WITH NOTES ON SPECIES ASSOCIATED WITH STORED FOOD AND HUMAN HABITATS AND A KEY TO SPECIES OF THIS GENUS ... 21

Abstract ... 21

a. Introduction ... 21

b. Material and Methods ... 21

c. Results ... 22

d. Discussion ... 32

References ... 38

3 REVISION OF THE GENUS Neotropacarus BAKER, 1985 (ASTIGMATINA: ACARIDAE) WITH DESCRIPTION OF THREE NEW SPECIES ... 43

Abstract ... 43

a. Introduction ... 43

b. Material and Methods ... 44

c. Results ... 44

References ... 70

4 DESCRIPTION OF TWO NEW GENERA AND SIX NEW SPECIES OF ACARID (ACARIDAE: HORSTIINAE) MITES ASSOCIATED WITH APID (HYMENOPTERA: APIDAE) BEES ... 43

Abstract ... 73

a. Introduction ... 73

b. Material and Methods ... 74

c. Results ... 74

References ... 109

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Abstract ... 113

a. Introduction ... 113

b. Material and Methods ... 115

c Results ... 116

d Discussion ... 118

e Conclusion ... 119

References ... 119

6 PRODUCTION OF THE HOUSE DUST MITES Blomia tropicalis BRONSWIJK, DE COCK AND OSHIMA (ECHIMYOPODIDAE) AND Dermatophagoides pteronyssinus (TROUESSART) (ASTIGMATINA: ECHIMYOPODIDAE; PYROGLYPHIDAE) ... 123

Abstract ... 123

a. Introduction ... 123

b. Material and methods ... 124

c. Results ... 127

d. Discussion ... 130

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RESUMO

Ácaros Astigmatina de vida livre (Astigmatina): novos táxons, criação e uso para a produção de ácaros predadores Mesostigmata

A coorte Astigmatina é dividida em dois grandes grupos: Psoroptidia, composto majoritariamente por ácaros de pena e pelos, e Não-Psoroptidia, componente dominante da acarofauna de habitats efêmeros. Nestes ambientes, os Astigmatina geralmente são saprófagos ou se alimentam de fungos e bactérias. Protoninfas de Astigmatina passam por uma completa reorganização da estrutura corporal levando à produção de deutoninfas heteromórficas geralmente especializadas para dispersão por forese utilizando artrópodes e vertebrados como forontes. Apesar de a maioria dos Astigmatina ocorrer em ambientes naturais, algumas espécies passaram a ocupar ambientes antrópicos, como depósitos de alimentos, onde algumas se tornaram pragas; alguns Astigmatina infestam órgãos subterrâneos de plantas. A despeito de sua importância econômica e ecológica, estudos sobre a diversidade e taxonomia dos Astigmatina no Brasil têm sido raros nas últimas décadas. O objetivo geral desta tese foi colaborar para o conhecimento da diversidade e avaliar o potencial de uso prático de espécies Astigmatina no Brasil. Para isso, novos gêneros e espécies foram descritos, métodos para criação de ácaros de poeira foram estudados e a eficiência de Astigmatina como presas para ácaros predadores edáficos foi avaliada. Uma nova espécie de Thyreophagus (Astigmatina: Acaridae) foi descrita com base em espécimes coletados no Brasil, uma revisão sobre três outras espécies deste gênero associadas com alimentos armazenados foi realizada e uma chave para todas as espécies deste gênero foi elaborada. O gênero Neotropacarus (Astigmatina: Acaridae), comumente associado a folhas de plantas, foi revisado, com redescrição de duas espécies e descrição de novas espécies coletadas no Brasil e nas Filipinas. Dois novos gêneros e sete novas espécies de Acaridae associados à família de abelha Apidae foram descritos e uma chave para os gêneros da subfamília Horstiinae foi elaborada. Diversas espécies de Astigmatina foram avaliadas como presas para os ácaros predadores Stratiolaelaps scimitus (Womersley) (Mesostigmata: Laelapidae) e Protogamasellopsis zaheri Abo-Shnaf, Castilho e Moraes (Mesostigmata: Rhodacaridae), que ovipositaram em todas os Astigmatina avaliados, sendo Tyrophagus putrescentiae (Schrank) e Aleuroglyphus ovatus (Tropeau) (Acaridae) as presas mais promissoras. Sete alimentos e dois períodos de desenvolvimento, 30 e 60 dias, após inoculação de 400 fêmeas de duas espécies importantes na poeira residencial, Blomia tropicalis van Bronswijk, de Cock e Oshima e Dermatophagoides pteronyssinus (Trouessart) foram avaliados. Com os alimentos mais adequados, o crescimento populacional nas colônias foram maiores que 20.2 e 15.3 para B. tropicalis e D. pteronyssinus, respectivamente.

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ABSTRACT

Free living astigmatid mites (Astigmatina): new taxa, rearing and use for Mesostigmata predatory mites production

The cohort Astigmatina is divided in two major groups: Psoroptidia, composed mainly by feather and fur mites, and Non-psoroptidia, a dominant component of the acarofauna in ephemeral habitats. In these environments Astigmatina usually are saprophages or feed on fungi or bacteria. Astigmatina protonymphs undergo a complete reorganization of the body structure leading to the production of heteromorphic deutonymphs, generally specialized for dispersion through phoresy using arthropods and vertebrates as phoronts. Although most Astigmatina occur in natural environments, some species live in anthropic environments, such as food deposits, where some of them became pests; some Astigmatina infest subterraneous plant organs. Despite their economic and ecological importance, studies on the diversity and taxonomy of Astigmatina in Brazil have been rare over the last decades. The general objective of this thesis was to collaborate to the knowledge of the diversity and to evaluate the potential practical uses of these mites in Brazil. For this, new genera and species were described, method for rearing dust mites was studied and the efficiency of Astigmatina as prey for edaphic predators was evaluated. A new species of Thyreophagus (Astigmatina: Acaridae) was described based on specimens collected in Brazil, the association of three other species of this genus with stored food was reviewed and a key to all species of this genus was prepared. The genus Neotropacarus (Astigmatina: Acaridae), commonly found on plant leaves, was reviewed with the redescription of two species and description of new species collected in Brazil and from the Philippines. Two new genera and seven new species of Acaridae associated with the bee family Apidae was described and a key to Acaridae genera in subfamily Horstiinae was prepared. Several species of Astigmatina were evaluated as prey for predatory mites Stratiolaelaps scimitus (Womersley) (Mesostigmata: Laelapidae) and Protogamasellopsis zaheri Abo-Shnaf, Castilho and Moraes (Mesostigmata: Rhodacaridae), which oviposited on all evaluated astigmatids, with Tyrophagus putrescentiae (Schrank) and Aleuroglyphus ovatus (Tropeau) (Acaridae) being the most suitable prey. Seven foods and two development period, 30 and 60 days, after the introduction of 400 females of two important dust mite species, Blomia tropicalis van Bronswijk, de Cock e Oshima and Dermatophagoides pteronyssinus (Trouessart) were evaluate. With the most suitable foods, the population growth were higher than 20.2 and 15.3 for B. tropicalis and D. pteronyssinus, respectively.

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1 INTRODUCTION

Astigmatina has been considered an order [Astigmata, by Evans, Sheals and

MacFarlaney (1961)] or suborder [Acaridida, by Krantz (1978) or Astigmata, by OConnor (1982a)]. Norton (1998) cited that 14 derived characters support the inclusion of Astigmatina in the suborder Oribatida, more specifically in the supercohort Desmonomatides. Therefore, Astigmatina is currently considered a Cohort within Oribatida (OConnor, 2009). Main morphological characteristics of feeding stages of Astigmatina are: body poorly sclerotized, except for a dorsal sclerite (more derived groups have heavily sclerotized body; e.g.

Guanolichidae and some Algophagidae); sejugal furrow retained in ancestral groups (lost in numerous derived groups); cuticle smooth or covered by striae or other forms of

ornamentation; many taxa with ventrally sclerotized coxal fields and reduced number of setae on legs I-IV; empodial claw usually present and well developed (absent or reduced in some groups); chelicerae are usually chelatedentate to crush solid food or act as scrapers (chelicerae highly modified to filter particles are present in Histiostomatoidea); rutella is diverse and cover most of the ventral apex of sucapitulum; stigmata or tracheal system are absent, so the respiration is presumed to be integumental; Grandjean´s organ, simple or very elaborated in shape, is found at the apex of the podecephalic sclerite; position of genital opening highly variable, ranging from far posterior and almost confluent with the anus to far between coxal fields I; two pairs of genital papillae usually present in postprotonymphal stages, may be absent in parasitic taxa (OConnor, 2009).

Astigmatina is divided in two major groups: one, a paraphyletic taxon composed by free-living species, and another, virtually monophyletic taxon, composed mostly by parasitic species (Psoroptidia) (OCONNOR, 2009). Non-psoroptidian groups differ from Psoroptidia by the presence of genital papillae (absent in Psoroptidia), tibia I-II with one or two tactile setae (c” always absent in Psoroptidia) and by the formation of heteromorphic deutonymph in several groups (always absent in Psoroptidia) (KRANTZ, 1978; OCONNOR, 2009).

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Non-psoroptidian Astigmatina are the most abundant component of the acarofauna in ephemeral habitats and may occur in dung, carrion, bat guano, nests of arthropods or other invertebrates, house dust, stored products, soil litter, plant foliage, flowers, caves and aquatic environments such as sap fluxes, phytotelmata and intertidal and to subtidial zones (OCONNOR, 2009).

In these environments Astigmatina usually are saprophages, but also feed on fungi or bacteria (OCONNOR, 2009). Within this group, most Histiostomatidae species are adapted to filter feeding (FASHING, 1998, 2010; KRANTZ, 1978; OCONNOR, 2009; WALTER; KAPLAN, 1990); more rarely Astigmatina may be predators of insects (BRUST; HOUSE, 1988; CANEVARI et al., 2012; HOUCK; COHEN, 1995; IZRAYLEVICH; GERSON, 1995; PAPADOPOULOU, 2006), other mites and nematodes (ABOU EL-ATTA; OSMAN, 2015; EKMEN et al., 2010; WALTER; HUDGENS; FRECKMAN, 1986). Some have developed the ability to consume vegetable tissue, especially bulbs and tubers (DÍAZ et al., 2000; MANSON, 1972; LESNA; SABELIS; CONIJN, 1996); fully aquatic species may consume algae (BÜCKING, 1999; FASHING; CAMPBELL, 1992).

Protonymphs of Astigmatina undergo a complete reorganization of the body structure leading to the formation of heteromorphic deutonymphs (OCONNOR, 2009). The most common heteromorphic type of deutonymph is specialized for dispersion, presenting a rudimentary gnathosoma, without mouth, extensive sclerotization and a caudoventral attachment organ (HOUCK; OCONNOR, 1991; OCONNOR, 2009). These features allow Astigmatina to disperse through phoresy using arthropods and vertebrates as phoronts and deutonymphal morphology is highly variable according to the phoront (FAIN, 1968, 1969, 1981; HOUCK; OCONNOR, 1991; VOLGIN, 1971).

A second type of deutonymph is specialized to resist unfavorable condition just waiting for the reestablishment of suitable temperature and humidity condition without moving to other places (HUGHES, 1976; HOUCK; OCONNOR, 1991; OCONNOR, 1994, 2009). These are called inert or regressive deutonymphs; they have even greater reduction of body appendices, legs and attachment organ becoming vestigial (calyptostase), and they remain within the protonymphal cuticle (eg. GRIFFITHS, 1966; HUGHES, 1955; van ASSELT, 2000).

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(WHITE; HENDERSON; SINHA, 1979), introduce fungi in the products (HUBERT et al., 2003) or affect the health of the workers, causing respiratory or cutaneous allergy (BLAINEY, 1989; CUTHBERT et al., 1979; IVERSEN et al., 1990). Some astigmatid species might infest subterraneous plants organs, such as bulb and tubercles, damaging the production of some important plants, as garlic, onion and ornamentals (DÍAZ et al., 2000; FAN; ZHANG, 2004).

Despite their economic and ecological importance, studies on the diversity and taxonomy of Astigmatina in Brazil have been rare over the last decades. As a result, the real diversity of species of this group both in natural and anthropic environments is not adequately known.

The motivation to the development of this thesis was: to contribute to the enhancement of the knowledge about the diversity of astigmatid mites in Brazil; to increase information about the use of astigmatid mites as factitious prey for mesostigmatid predators and to provide preliminary results to the development of methods for mass production of house dust mites.

Thus, the specific objectives of this thesis were:

 To provide the description of a new species of Thyreophagus (Acari: Acaridae) collected in Piracicaba, Brazil, a key for species of this genus and to discuss the importance of Thyreophagus species as stored food pests;

 To review the genus Neotropacarus (Acaridae: Acaridae), redescribing two species and describing three new species of this genus, as well as providing a key to the species of this genus;

 To describe two new genera and seven new species of Acaridae associated with Apidae bees;

 To evaluate the efficiency of Astigmatina species as factitious prey for rearing edaphic predadors;

 To assess the potential of different foods and two development period for production of two species of house dust mite.

References

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Tyrophagus putrescentiae (Acari: Acaridae) on plant-parasitic nematodes and artificial diets.

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BLAINEY, A.D.; TOPPING M.D, OLLIER S., DAVIES R.J. Allergic respiratory disease in grain workers: The role of storage mites. Journal of Allergy and Clinical Immunology, Saint Louis, v. 84, n. 3, p. 296-303, 1989.

BOCHKOV, A. Morphological adaptations of acariform mites (Acari: Acariformes) to permanent parasitism on mammals. Parazitologiia, St. Petersburg,v. 41, n. 6, p. 428-458, 2006.

BRUST, G.E.; HOUSE, G.J. A study of Tyrophagus putrescentiae (Acari: Acaridae) as a facultative predator of southern corn rootworm eggs. Experimental and Applied Acarology,

Amsterdam, v. 4, n. 4, p. 335-344, 1988.

BÜCKING, J. Population biology of a phytophagous mite of marine and estuarine rocky shores (Astigmata, Hyadesiidae). In: BRUIN, J.; VAN DER GEEST, L.P.S.; SABELIS, M.W. (Ed.). Ecology and Evolution of the Acari. New York: Springer, 1999. chap. 36, p. 441-450.

CANEVARI, G.C.; REZENDE, F.; SILVA, R.B; FARONI, L.R.D.; ZANUNCIO, J.C.; PAPADOPOULOU, S.; SERRÃO, J.E. Potential of Tyrophagus putrescentiae (Schrank) (Astigmata: Acaridae) for the biological control of Lasioderma serricorne (F.) (Coleoptera: Anobiidae). Brazilian Archives of Biology and Technology, Curitiba, v. 55, n. 2, p. 299-303, 2012.

CUTHBERT, O.D.; BROSTOFF J.; WRAITH, D.G.; BRIGHTON, W.D. Barn allergy: asthma and rhinitis due to storage mites. Clinical & Experimental Allergy, Oxford, v. 9, n. 3, p. 229-236, 1979.

DÍAZ, A.; OKABE, K.; ECKENRODE, C.J.; VILLANI, M.G.; OCONNOR, B.M. Biology, ecology, and management of the bulb mites of the genus Rhizoglyphus (Acari: Acaridae).

Experimental and Applied Acarology, Amsterdam, v. 24, n. 2, p. 85-113, 2000.

EKMEN, Z.I.; CAKMAK, I.; KARAGOZ, M.; HAZIR, S.; OZER, N.; KAYA, H.K. Food preference of Sancassania polyphyllae (Acari: Acaridae): living entomopathogenic nematodes or insect tissues? Biocontrol Science and Technology, Oxford, v. 20, n. 6, p. 553-566, 2010.

EVANS, G.O.; SHEALS, J.G.; MACFARLANE, D. The terrestrial acari of the British Isles: an introduction to their morphology, biology and classification. London: British Museum, 1961. 219 p.

FAIN, A. A new heteromorphic deutonymph (hypopus) of a sarcoptiform mite parasitic under the skin of a toucan. Journal of Natural History, London, v. 2, n. 4, p. 459-461, 1968.

______. Adaptation to parasitism in mites. Acarologia, Paris, v. 11, n. 3, p. 429-449, 1969.

______. A revision of the phoretic deutonymphs (hypopi) of the genus Sennertia Oudemans, 1905 (Acari, Astigmata, Chaetodactylidae). Systematic Parasitology, Dordrecht, v. 3, n. 3, p. 145-183, 1981.

FAN, Q-H.; ZHANG, Z-Q. Revision of Rhizoglyphus Claparède (Acari: Acaridae) of

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FASHING, N.J. Functional morphology as an aid in determining trophic behaviour: the placement of astigmatic mites in food webs of water-filled tree-hole communities.

Experimental and Applied Acarology, Amsterdam, v. 22, n. 8, p. 435-453, 1998.

______. Life history and biology of Hormosianoetus mallotae (Fashing) (Histiostomatidae: Astigmata), an obligatory inhabitant of water-filled treeholes. International Journal of Acarology, Oak Park,v. 36, n. 3, p. 189-198, 2010.

FASHING, N.J.; CAMPBELL, D.M. Observations on the feeding biology of Algophagus pennsylvanicus (Astigmata: Algophagidae), a mite restricted to water-filled treeholes.

International Journal of Acarology, Oak Park, v. 18, n. 2, p. 77-81, 1992.

GRIFFITHS, D.A. Nutrition as a factor influencing hypopus formation in the Acarus siro species complex (Acarina, Acaridae). Journal of Stored Products Research, Oxford,v. 1, n. 4, p. 325-340, 1966.

HOUCK, M.A.; COHEN, A.C. The potential role of phoresy in the evolution of parasitism: radiolabelling (tritium) evidence from an astigmatid mite. Experimental and Applied Acarology, Amsterdam, v. 19, n. 12, p. 677-694, 1995.

HOUCK, M.A.; OCONNOR, B.M. Ecological and evolutionary significance of phoresy in the Astigmata. Annual Review of Entomology, Stanford,v. 36, n. 1, p. 611-636, 1991.

HUBERT, J.; STEJSKAL, V.; KUBÁTOVÁ, A.; MUNZBERGOVÁ, Z.; VÁNOVÁ, M.;

ŽDÁRKOVÁ, E. Mites as selective fungal carriers in stored grain habitats. Experimental and Applied Acarology, Amsterdam, v. 29, n. 1/2, p. 69-87, 2003.

HUGHES, A.M. On the inert hypopial form of Acarus siro L. (= Tyroglyphus farinae L.). (Acarina). The Entomologist's Monthly Magazine, Oxford, v. 91, p. 99-102, 1955.

______. The mites of stored food and houses. London: Ministry of Agriculture and Fisheries, 1976. 400 p. (Technical Bulletin, 9).

IVERSEN, M.; KORSGAARD, J.; HALLAS, T.; DAHL, R. Mite allergy and exposure to storage mites and house dust mites in farmers. Clinical and Experimental Allergy, Oxford, v. 20, n. 2, p. 211-219, 1990.

IZRAYLEVICH, S.; GERSON, U. Host scale effects on the parasitic mite Hemisarcoptes coccophagus Meyer and their implications for the biological control of diaspidid pests. Israel Journal of Entomology, Tel Aviv, v. 29, p. 291-296, 1995.

KRANTZ, G.W. A manual of acarology. 2nd ed. Corvallis: Oregon State University Bookstores, 1978. 509 p.

LESNA, I.; SABELIS, M.; CONIJN, C. Biological control of the bulb mite, Rhizoglyphus robini, by the predatory mite, Hypoaspis aculeifer, on lilies: predator-prey interactions at various spatial scales. Journal of Applied Ecology, Oxford, v. 33, n. 2, p. 369-376, 1996.

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OCONNOR, B.M. Evolutionary origins of astigmatid mites inhabiting stored products. In: RODRIGUEZ, J.G. (Ed.). Recent Advances in Acarology. Cambridge: Academic Press, 1979. p. 273-278.

______. Astigmata. In: PARKER, S.P. (Ed.). Synopsis and classification of living

organisms. New York: McGraw-Hill, 1982a. p. 146-169.

______. Evolutionary ecology of astigmatid mites. Annual Review of Entomology, Stanford, v. 27, n. 1, p. 385-409, 1982b.

______. Life-history modifications in astigmatid mites.In: HOUCK, M.A. (Ed.). Mites:

ecological and evolutionary analyses of life-history patterns. New York: Springer, 1994. chap. 6, p. 136-159.

______. Cohort astigmatina. In: KRANTZ, G.W.; WALTER, D.E. (Ed.). A Aanual of Acarology. Lubbock: Texas Tech University Press, 2009. chap. 16, p. 565-657.

PAPADOPOULOU, S.C. Tyrophagus putrescentiae (Schrank) (Astigmata: Acaridae) as a new predator of Lasioderma serricorne (F.) (Coleoptera: Anobiidae) in tobacco stores in Greece. Journal of Stored Products Research, Oxford, v. 42, n. 3, p. 391-394, 2006.

PROCTOR, H.C. Feather mites (Acari: Astigmata): ecology, behavior, and evolution. Annual Review of Entomology, Stanford, v. 48, n. 1, p. 185-209, 2003.

SOLOMON, M.E. Tyroglyphid mites in stored products. Nature and amount of damage to wheat. Annals of Applied Biology, Warwick, v. 33, n. 3, p. 280–289, 1946.

van ASSELT, L. Observations on the life cycle of Chaetodactylus osmiae (Dufour, 1839) (Acari: Chaetodactylidae) parasitic on the solitary bee, Osmia rufa (L.), 1758 (Insecta:

Hymenoptera) in Belgium. International Journal of Acarology, Oak Park, v. 26, n. 3, p. 221-228, 2000.

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WALTER, D.E.; HUDGENS, R.A.; FRECKMAN, D.W. Consumption of nematodes by fungivorous mites, Tyrophagus spp. (Acarina: Astigmata: Acaridae). Oecologia, Berlin,v. 70, n. 3, p. 357-361, 1986.

WALTER, D.E.; KAPLAN, D.T. Feeding observations on two astigmatic mites, Schwiebea rocketti (Acaridae) and Histiostoma bakeri (Histiostomatidae) associated with Citrus feeder roots. Pedobiologia, Jena,v. 34, n. 5, p. 281-286, 1990.

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2 A NEW SPECIES OF Thyreophagus (ACARI: ACARIDAE) FROM BRAZIL,

WITH NOTES ON SPECIES ASSOCIATED WITH STORED FOOD AND HUMAN HABITATS AND A KEY TO SPECIES OF THIS GENUS

Abstract

A new species Thyreophagus n. sp. is described morphologically based on adult females, adult homeomorphic and heteromorphic males collected from chicken feed in Brazil. The Thyreophagus species associated with stored food and human habitats are reviewed, and a key to separate species of this genus is provided.

Keywords: Taxonomy; Stored food mites; Thyreophagus

a. Introduction

Most species of the genus Thyreophagus Rondani, 1874 are associated with insects or subcortical environments (FAIN, 1982), but some species are known to occur in house dust and in stored food, sometimes damaging these products (FAIN, 1982; HUGHES, 1976). One species of this genus Thyreophagus entomophagus (Laboulbène) has been reported to affect human health when ingested (BLANCO et al., 1997; IGLESIAS-SOUTO et al., 2009; SÁNCHEZ- MACHÍN et al., 2010).

A new species of Thyreophagus was recently found in southeastern Brazil. The aim of this work is to describe this new species based on morphological characters of adult females and males, to summarize information about Thyreophagus species from human habitats and stored food, and to provide a key to separate species of this genus.

b. Material and Methods

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OConnor (2009), which is based on the system developed by Grandjean (1939) and applied to the Astigmatina by Griffiths et al. (1990). Leg chaetotaxy also follows that proposed by OConnor (2009).

c. Results

Systematics

Thyreophagus Rondani

Thyreophagus Rondani, 1874: 67 [type species Thyreophagus entomophagus Rondani, 1874 (=Acarus entomophagus Laboulbène, 1852, by monotypy]; Zachvatkin 1940: 43; Zachvatkin 1941: 208; Türk & Türk 1957: 145 (part); Mahunka 1974: 374 (part); Hughes 1976: 123; Chmielewski 1977: 65 (part); Fain 1982: 7; Bugrov 1997: 151; Klimov 1998: 4.

Monieziella Berlese, 1897: 107 (part) [type species Monieziella entomophaga (Laboulbène, 1852) (= Thyreophagus entomophagus), by subsequent designation (Jacot 1936)]; Jacot 1936: 628 (part). Synonymized by Fain & Johnston (1974).

Fumouzea Zachvatkin, 1953: 57 [type species Fumouzea entomophaga (Laboulbène 1852) (=Thyreophagus entomophagus Laboulbène, 1852), by monotypy]. Synonymized by Klimov (1998).

Michaelopus Fain and Johnston, 1974: 411 [type species Tyroglyphus corticalis Michael, 1885, by original designation]; Fain 1982: 18; Cruz 1990: 1; Sevastianov & Kivganov 1992: 25. Synonymized by Halliday (1998).

Thyreophagus n. sp. (Figs. 1–5)

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Figure 1 - Thyreophagus n. sp. (female). (A) Dorsal view. (B). Ventral view

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chelate, 79 (72–83), fixed digit 23 (19–27), with 3 teeth in addition to apical tooth; movable digit 25 (23–27) long, with 2 teeth in addition to apical tooth; cheliceral seta (cha) spine-like, 3 (2–4) long. Subcapitular seta (subc) 22 (18-26) long, palp tibial seta spine-like; lateral palp tibial seta setiform; dorsal palp tarsal seta setiform and terminal palp tarsal solenidion minute; seta elcp setiform, 12 (9–13).

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Figure 3 -Thyreophagus n. sp. (female). Photomicrography of the reproductive apparatus

Legs (Figs. 4A-K): Leg I 105 (90 – 110) long; tarsus with 4 apical spine-like setae [1 dorso-apical and 3 ventral (2 dorso-apical and 1 subdorso-apical)], 3 solenidion and 4 setiform tactile setae; tibia with 1 solenidion and 2 setiform tactile setae; genu with 2 solenidion and 2 setiform tactile setae; femur with 1 setiform tactile seta; trochanter with 1 setiform tactile seta. Lengths of solenidion: ω1 curved, distally swollen, 12 (10 14), ω2 5 (4–7), ω3 14 (12–18), φ 68 (59–72), σ’

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Figure 4 - Thyreophagus n. sp. (female). (A) Leg I. (B) Tarsus I—dorsal view. (C) Tarsus I—ventral view. (D) Leg II. (E) Tarsus II—dorsal view. (F) Tarsus II—ventral view. (G) Leg III. (H) Tarsus III—dorsal view. (I) Tarsus III—ventral view. (J) Leg IV. (K) Tarsus IV—dorsal view. (L) Tarsus IV—ventral view

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(21–26), ex 32 (27–33), cp 22 (18–24), d2 14 (12–19), e2 20 (16–23), h1 14 (10–16) and h2 28 (22–32).

Figure 5 - Thyreophagus n. sp. (homeomorphic male). (A) Dorsal view. (B). Ventral view

Venter (Figs. 5B, 6B): Aedeagus slightly curved, 8 (6–12) long, between coxae IV; h3 44 (38 – 49) long. Para-anal suckers 10 (9–10) in diameter surrounded by 3 pairs of paraproctal setae: p1, posteriad of each sucker, 5 (4–5) long; p2 laterad of suckers and 5 (4 – 5) long; and p3, anteriad of suckers and vestigial.

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Legs (Figs. 7A–L): Leg I 71 (67–82) long; tarsus with 4 apical spine-like setae [1 dorso-apical and 3 ventral (2 dorso-apical,and 1 subdorso-apical)], 3 solenidion and 4 setiform tactile setae; tibia with 1 solenidion and 2 setiform tactile setae; genu with 2 solenidion and 2 setiform tactile setae; femur with 1 setiform tactile seta; trochanter with 1 setiform tactile seta. Lengths of solenidion: ω1 6 (5–9), ω2 4 (4–5), ω3 4 (2–6), φ 44 (34–47), σ’ 11 (10 – 16), σ’’ 6 (5 – 7). Leg II 60 (53–76) long; tarsus with 4 apical spine-like setae [1 dorso-subapical and 3 ventral (2 apical and 1 subapical)], 1 solenidion and 4 setiform tactile setae; tibia with 1 solenidion and 2 setiform tactile setae; genu with 1 solenidion and 2 setiform tactile setae; femur with 1 setiform tactile seta; trochanter with 1 setiform tactile seta. Lengths of solenidion: ω1 7 (6–7),

φ42 (33–52), σ 3 (3–4). Leg III 51 (42–57) long; tarsus with 7 apical spine-like setae [1 dorso-subapical and 6 ventral (4 apical, 1 dorso-subapical and 1 median)]; tibia with 1 solenidion and 1 setiform tactile seta; genu and femur without seta; trochanter with one setiform tactile seta; solenidion φ 43 (40–47) long. Leg IV 57 (53–64); tarsus with 4 apical spine-like setae [1 dorso-subapical and 3 ventral (2 apical and 1 subapical)], 2 setiform tactile setae and 2 suck-like setae; solenidion φ 5 (4–5) long.

Figure 6 - Thyreophagus n. sp. (homeomorphic male) (A) Prodorsal sclerite. (B) Genital region

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cheliceral seta (cha) 3 (2–3). Subcapitular seta (subc) 19 (16–20) long; supracoxal seta elcp 9 (8

– 9) long.

Dorsum: Prodorsal sclerite 66 (62–68) and 49 (44–53) wide at anterior margins; supracoxal seta (elc I) 14 (12–16). Dorsal idiosomal setae lengths: ro 26 (22–29), ex 47 (41–53), cp 37 (29–

38), d2 24 (19 26), e2 30 (24–33), h1 22 (18–24) and h2 36 (32–42). Venter: Aedeagus 8 (6–12) long. Para-anal suckers 11 in diameter, h3 44 (38–49), p1 and p2 3 (3–4) and 5 (4–6) long, respectively, p3 vestigial. Legs (Figs. 7M–O): Legs I–II and IV similar to homeomorphic male. Leg I 105 (87 – 110) long; lengths of solenidion: ω1 10 (9–10), ω2 5 (4–7), ω3 4 (2–6), ε 3 (2–3), φ 60 (54–67), σ’ 18 (16–20), σ’’ 10 (8–12). Leg II 96 (83– 105) long; lengths of solenidion: ω 8 (6–9); φ 61 (59–62); σ 3 (2–3). Leg III 71 (63 – 78) long, with 2 thick dorso-apical spines and 3 ventral spine-like setae (2 apical and 1 subapical); φ 55 (51–59) long. Pretarsus III absent. Leg IV 67 (61–72) long, φ 4 (3–5).

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Figure 7 - Thyreophagus n. sp. (A–L homeomorphic male; M–O heteromorphic male). (A) Leg I. (B) Tarsus I— dorsal view. (C) Tarsus I—ventral view. (D) Leg II. (E) Tarsus II—dorsal view. (F) Tarsus II—ventral view. (G) Leg III. (H) Tarsus III—dorsal view. (I) Tarsus III—ventral view.(J) Leg IV. (K) Tarsus IV— dorsal view. (L) Tarsus IV—ventral view. (M) Leg III. (N) Tarsus III—dorsal view. (O) Tarsus III— ventral view

Type material. Holotype female, 15 female, 16 heteromorphic male and 3 homeomorphic male paratypes from chicken feed, BRAZIL: São Paulo state, Piracicaba, 6 April 2012, coll. M. F. C. Barbosa.

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homeomorphic male are deposited at the University of Michigan Museum of Zoology (UMMZ), Ann Arbor, Michigan, USA.

Remarks. The genus Thyreophagus is known from adults and heteromorphic deutonymphs.

Thyreophagus n. sp. is the second species of this genus reported from Brazil and the first described as new from this country. This new species strongly resembles T. tridens (FAIN; LUKOSCHUS, 1986) by having similar body length, prodorsal sclerite and having most dorsal setae similar in length. In addition, T. tridens has the spermathecal sclerite arched and the same number of spine-like setae on tarsi of legs I–IV as Thyreophagus n. sp. However, T. tridens differs from Thyreophagus n. sp. by having a different pattern of punctation on the prodorsal sclerite (punctate on its anterior two thirds or three quarters and fine striations on the rest of the sclerite) and smaller φ III and φ IV (1.7 and 3.5 times smaller, respectively).

This new species resembles Thyreophagus spinitarsis (FAIN, 1982) by having similar patterns on the prodorsal sclerite. The latter differs from Thyreophagus n. sp. by having the idiosoma about 1.9 times as long, most of the dorsal idiosomal setae about 1.5 times as long and by having the sclerotized base of the spermatheca approximately bell-shaped.

Thyreophagus australis Clark, 2009 is similar to this new species by having Grandjean´s organ anteriorly expanded in membranous finger-like extensions and the male without any projection or sclerite on the posterior opisthosomal region. However, T. australis differs by having females with the idiosoma globose instead of elongate, setae ro and ex more than four times longer and the sclerotized base of the spermatheca as a transverse band. Thyreophagus gallegoi gallegoi Fain, 1982 resembles this new species by having the idiosoma and dorsal setae of about the same lengths, similar shape of sclerotized base of spermatheca and by producing heteromorphic males. This subspecies differs by ω1 strongly curved and thin apically and the prodorsal sclerite mostly covered by uniformly fine striae.

d. Discussion

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in the field, or the predatory mites may be quantified and placed in standardized numbers in units containing the same substrate and the acarid prey for field release (GERSON et al., 2003). The species described here, Thyreophagus n. sp., was found on stored human and animal food in Piracicaba, São Paulo State, Brazil. Besides chicken feed, the substrate from which the population used for the present description was collected, this species was also found in soy and corn flours. In addition, colonies of this species were successfully kept in the laboratory on yeast, wheat germ, cornmeal and oatmeal. Thyreophagus n. sp. was evaluated as prey for species of Phytoseiidae (the predatory mite family most widely used for biological control of plant inhabiting pests) and Laelapidae (commonly used for control of edaphic pests) in our laboratory. The results showed a high potential of Thyreophagus n. sp. as alternate prey for mass rearing the evaluated phytoseiid and laelapid species. Barbosa and Moraes (2015) reported details of the efficiency of Thyreophagus n. sp. as factitious prey for mass rearing phytoseiids.

Thyreophagus entomophagus, a cosmopolitan synanthropic species, has been collected mostly in association with insects and from stored food (FAIN, 1982). Hughes (1976) mentioned this species as an inhabitant of storehouses containing grain, flour, animal feed, etc. This is one of the most common mites found infesting foods and the only species of the genus reported to cause anaphylaxis when ingested (DUTAU, 2002; SÁNCHEZ-BORGES et al., 2013). In Spain, this species is the main cause of oral allergies (SÁNCHEZ-BORGES et al., 2013), being reported to cause anaphylaxis in several cases (BLANCO et al., 1997; IGLESIAS-SOUTO et al., 2009; SÁNCHEZ-MACHÍN et al., 2010). Anaphylaxis caused by this mite was also reported in the southern Brazilian state of Santa Catarina (MAZZUCCO et al., 2000).

Thyreophagus gallegoi was reported from house dust in Spain (FAIN, 1982; PORTUS; GOMEZ, 1979) and China (FAN et al., 2010; JIANG, 1991). It was also reported from wheat flour in Spain (PORTUS; GOMEZ, 1979) and intercepted in the USA from bean curd originating from Hong Kong and from the Philippines and from hoisin sauce from Hong Kong (OLSEN, 1983). Thyreophagus macfarlanei (FAIN, 1982) is known only from its type specimens, collected on wheat in England (FAIN, 1982).

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Key to species of Thyreophagus.

Adults of the following species are unknown: T. africanus Mahunka, 1974, T.

sminthurus (Fain and Johnston, 1974), T. johnstoni (Fain, 1982), T. leclercqi (Fain, 1982) and T. rwandanus (Fain, 1982).

The following species are inadequately described and are not included in this key: T. angustus (Banks, 1906), T. berlesiana (Zachvatkin, 1941), T. lignieri (Zachvatkin, 1953), and T. magna (Berlese, 1910). Thyreophagus cercus Zhang, 1994 should probably be transferred to the genus Reckiacarus.

FEMALES

1. Very large species, body length > 1500 µm; Egypt . . . . . . T. cynododactylon El-Bishlawy, 1990

1’. Smaller species, body length < 700 µm . . . . . . .2. 2. Tarsi III with 4 apical spine-like setae, 1 dorsal (ft") and 3 ventral [s, (u)], proral setae vestigial or absent, and 3-4 filiform setae (seta pv" III filiform, setiform or absent) . . . .. . . ..3.

2’. Tarsus III with 6 or 7 well developed, apical, spine-like setae (proral seta distinct) and 3 or 4 simple setae (seta pv"III filiform or spine-like); tarsus IV with 6 spine-like setae and 4 simple setae . . . ……… . . . 5. 3. Prodorsal sclerite wider than long, almost entirely punctate, with a few short longitudinal striae in posteromedian region; sclerite of spermatheca in form of an inverted bell, with base 18-20 µm wide; tarsus III with seta pv" filiform; solenidion ω1 of tarsus I narrowed apically; posterior ventral seta (c") of tibiae I–II setiform about 5 µm long; widespread. . .

. . . ………. . . T. entomophagus (Laboulbene, 1852)

3’. Prodorsal sclerite clearly longer than wide, almost entirely covered with fine longitudinal striae; sclerite of spermatheca not in form of a bell, and smaller; tarsus III with pv" as small spine-like seta or absent; solenidion ω1 of tarsus I expanded apically; posterior ventral seta of tibiae I–II tiny and spine-like or absent . . . 4. 4. Idiosomal length 270-360 µm, width 87–150 µm, sclerite of spermatheca very small, slightly wider (6 µm) than long (5 µm) and not narrowed toward its center; seta pv" of tarsus III very short and spine-like; tibiae I–II without posterior ventral seta; Morocco

………...……….. . . .. .. . T. cooremani Fain, 1982

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narrowed toward middle and widened proximally; seta pv" of tarsus III absent; tibiae I–II with aposterioventral tiny spine-like seta (c"); Europe . . . T. odyneri Fain, 1982 5. Tarsus III with 7 spine-like and 3 simple setae; prodorsal sclerite mostly covered by fine, longitudinal striae except in 1 species where sclerite punctate . .. . . .. . . …. . . .6.

5’. Tarsus III with 6 spines and 4 simple setae; prodorsal sclerite almost entirely punctate; longitudinal striae confined to posterior quarter of sclerite or absent………….. . . . . . . 13. 6. Prodorsal sclerite entirely punctate, without linear striae . . . . . . . …….... . . .. . .7.

6’. Prodorsal sclerite with at least some portion bearing linear striae (striae very short in Thyreophagus n. sp.) . . . . . ………... . . . . . 8. 7. Prodorsal sclerite with posterior median lobe; posterior hysterosomal seta h1 less than half as long as h2; Colombia . . . . . . T. incanus (Fain, 1987)

7’. Prodorsal sclerite broadly rounded posteriorly; hysterosomal setae h1 and h2 elongate, similar in length; New Zealand. . . . . . .. . . T. australis Clark, 2009 8. With 1 pair of large, sclerotized, funnel-like, internal structures near posterior end of body (not to be confused with small, bellshaped structures at base of spermatheca) . .. . . .9.

8’. Without paired, funnel-like inner, posterior structures……... . . . 10. 9. Solenidion ϕ of tibia IV very short (4 µm); USA, California . . . .. . . . . . .. . . .. . . . T. tridens (Fain and Lukoschus, 1986)

9’. Solenidion ϕ of tibia IV longer (14 µm); Brazil . . . .. . . Thyreophagus n. sp 10. Prodorsal sclerite with linear striae restricted to posterior half of sclerite; Great Britain . . . ……….. . . .T. vermicularis Fain and Lukoschus, 1982

10’. Prodorsal sclerite with linear striae extending over at least 75% of its length . …… . 11. 11. Base of spermatheca with sclerite in form of a broad arc, much wider than long; widespread . . . .. . . . T. gallegoi Portus and Gomez, 1979

11’. Base of spermatheca with sclerite not wider than long. . . 12. 12. Base of spermatheca with sclerite quadrate, about as long as wide; Europe . . . . . . .. . . .T. spinitarsus (Fain, 1982)

12’. Base of spermatheca with sclerite at least three times longer than wide; Europe . . . . . . .. . . .. . . T. corticalis Michael, 1885. 13. Tarsi I–II with 4 spine-like setae (pv' absent); solenidion σ' and σ" of genu I similar in length; Ukraine . . . .. . . T. annae (Sevastianov and Kivganov, 1992)

13’. Tarsi I–II with 5 spine-like setae (pv' present); solenidion of genu I dissimilar in length

………..14.

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14’. Tibiae I–II with 1 seta (c" absent) . . . .. . . . . . 16. 15. Prodorsal sclerite with narrow, posterior lobe bearing longitudinal striae; anterior margin of sclerite with paired lateral indentations; Ireland . . . .. . . T. evansi (Fain, 1982)

15’. Prodorsal sclerite smoothly rounded posteriorly, without distinct posterior, striated lobe; anterior margin of sclerite without paired indentations; Cuba . . . T. passerinus (Cruz, 1990) 16. Long terminal setae h2 and h3 with bases inflated, conical; spermathecal sclerite forming thin sclerotized arc divided anteriorly into 4 short, fine sclerotized lines; genu I with

σ’ and σ” with 8 and 6 µm long, respectively (ratio 1.4:1); Great Britain. .

………...T. macfarlanei (Fain, 1982)

16’. Long terminal setae h2 and h3 with very thin bases; spermathecal sclerite forming a U-shaped structure with thick sides, 6 µm long, 5 µm wide; genu I with σ’ and σ” with 18-20 and 12 µm long, respectively (ratio 1.58: 1); Morocco . . . T. athiasae (Fain, 1982)

MALES

Males unknown or inadequately described in T. athiasae, T. cooremani, T. evansi, T. macfarlanei, T. spinitarsis, T. tridens, and T. vermicularis.

1. Prodorsal sclerite punctate………. . . . 2

1’. Prodorsal sclerite with short longitudinal striae, at least near posterior margin ……. . 5. 2. Posterior venter with sclerotized projection very poorly developed or absent; Colombia . . . .. . . .. . T. incanus (Fain, 1987)

2’. Posterior venter with sclerotized projection well developed . . . .. . . 3. 3. Body 6 times longer than wide; large species (> 700 µm); Egypt . . . . . . .. . . T. cynododactylon El-Bishlawy, 1990

3’. Body ovoid, 1.5–2 times longer than wide; (< 500 µm); widespread . . . . . . .. . . 4. 4. Tarsus IV with 5 spine-like setae [s, (p), (u)], 3 filiform setae [(pv), tc']; Ireland . . . . . . . .. . . .. . . T. evansi (Fain, 1982)

4’. Tarsus IV with 3 spine-like setae [s, (u)] (proral setae vestigial or absent), 3 filiform setae [(pv), tc']; widespread . . . .. . T. entomophagus (Laboulbène, 1852) 5. Posterior body with distinct sclerotized projection . . . . . .6.

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6’. Longitudinal striae on prodorsal sclerite restricted to median region, lateral areas simply punctate; tarsus IV with 5 spinelike setae (proral setae distinct); Europe . . . . . . .. . . T. corticalis (Michael, 1885)

7. Posterior hysterosoma with a large sclerotized area extending posteriad from level of setae e2; Ukraine . . . .. . . . .. . . .. . . T. annae (Sevastyanov and Kivganov, 1992)

7’. Posterior hysterosoma unsclerotized or at most with short terminal sclerotization posterior to setae h1. . . .. . . .. .. . . 8. 8. Posterior idiosoma with short sclerotized area posterior to setae h1 . .. .. . . . . . .9.

8’. Posterior idiosoma unsclerotized . . . . .. . . .. . . 10. 9. Genu I with solenidion σ' and σ" approximately equal in length; widespread . . . . . . . . . T. gallegoi Portus and Gomez, 1979

9’. Genu I with solenidion σ ' only half of length of σ"; Cuba . . . .. T. passerinus (Cruz, 1990) 10. Dorsal hysterosomal setae relatively long, setae d2 and e2 much longer than distance between their alveoli; New Zealand . . . .T. australis Clark, 2009

10’. Dorsal hysterosomal setae much shorter, setae d2 and e2 shorter than distance between their alveoli; Brazil .. . . ……… . . Thyreophagus n. sp.

DEUTONYMPHS

Translated and updated from Fain (1982)

Deutonymphs of the following species are unknown: T. annae (Sevastianov and Kivganov, 1992), T. athiasae (Fain, 1982), T. cynododactylon El-Bishlawy, 1990, T. cooremani Fain, 1982, Thyreophagus n. sp., T. evansi (Fain, 1982), T. gallegoi Portus and Gomez, 1979, T. incanus (Fain, 1987), T. macfarlanei (Fain, 1982), T. odyneri Fain, 1982, T. spinitarsus (Fain, 1982), T. tridens (Fain and Lukoschus, 1986), and T. vermicularis Fain and Lukoschus, 1982.

1. Dorsal surface completely striated; Afrotropical . . . . . . . T. africanus Mahunka, 1974

1’. Dorsal surface smoothly punctate, without striae . .. . . . .. . . . ……. . . .2. 2. Body ovoid, 1.3–1.5 times longer than wide . . . .. . . ... . . . . .3.

2’. Body elongate, more than 1.7 times longer than wide . . . . .. . . .. . . 5. 3. Tibiae I–II with posterior seta (c") more than half the length of anterior ventral seta (v'); Europe . . . .. . . …..……… T. leclercqi (Fain, 1982)

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4. Opisthonotal gland openings approximately equidistant from setae c3 and cp; widespread . . . .. . . T. entomophagus (Laboulbène, 1852)

4’. Opisthonotal gland openings much closer to ventral seta c3 than to dorsolateral seta cp; New Zealand . . . . . . …….. . . T. australis Clark, 2009 5. Tibiae I–II with only 1 ventral seta (v'), posterior seta c" absent; Great Britain . . . . . . .. . . T. sminthurus (Fain and Johnston, 1974)

5’. Tibiae I–II with 2 ventral setae, v' and c" present . .. . . .6. 6. Tibia II both ventral setae (v', c") in the form of short spines similar in length; ocelli relatively small (width 8.5–9 µm); Afrotropical. . . .. . . T. rwandanus (Fain, 1982)

6’. Tibia II with anterior ventral seta (v') setiform to filiform, twice of length of spine-like posterior ventral seta (c"); ocelli larger (width 12–19 µm) . . . .. . . .7. 7. Width of ocellus about 19 µm, distance between ocelli about 60 µm; hysterosomal sclerite about 2 times longer than prodorsal sclerite; widespread. . . T. corticalis (Michael, 1885)

7’. Width of ocellus about 12 µm, distance between ocelli about 42 µm; hysterosomal sclerite about 1.7 times longer than prodorsal sclerite; Nearctic. . .. . . . T. johnstoni (Fain, 1982)

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3 REVISION OF THE GENUS Neotropacarus BAKER, 1985 (ASTIGMATINA:

ACARIDAE) WITH DESCRIPTION OF THREE NEW SPECIES

Abstract

The genus Neotropacarus is revised. Two species, Neotropacarus bakeri (Collyer, 1966) and Neotropacarus mumai (Cunliffe, 1964), are redescribed and three new species, Neotropacarus n. sp. 1, Neotropacarus n. sp. 2and Neotropacarus n. sp. 3, are described from specimens from plant leaves and bird nests collected in Brazil and the Philippines

Keywords: Taxonomy; Neotropacarus; Acaridae

a. Introduction

Cunliffe (1964) established the genus Tropacarus based on a single species, Tropacarus mumai Cunliffe. A few years later, Baker (1985) renamed it as Neotropacarus, because that name was preoccupied by Tropacarus Ewing, 1917 (Acari: Oribatida). Neotropacarus was placed by Klimov (2000) in Caloglyphini, Acaridae.

The original diagnosis of Neotropacarus was based on specimens collected by E. W. Baker from various unidentified plants in the Democratic Republic of Congo (mentioned as Congo). Cunliffe (1964) reported that besides the type locality, Neotropacarus mumai (Cunliffe, 1964) had also been found in “Florida, Costa Rica, Nicaragua, India, and Brazil (U.S.

Quarantine)”. Since then, this species has been found on plants of different families from

several tropical and subtropical regions. The only other species of this genus, Neotropacarus bakeri (Collyer, 1966), was described from New Zealand from 16 plant species and the only additional record of this species was published by Zhang (2012).

The morphology of Neotropacarus is known only from adult females and homeomorphic adult males; heteromorphic deutonymphs were never reported (KLIMOV, 2000). These mites are found in clusters that include eggs, juveniles and adults on the abaxial leaf surface, often in light depressions, where they feed on fungi (MUMA, 1961). If the colonies are disturbed, they move clumsily until a new hiding place is found or the cluster is reallocated. Collyer (1966) reported N. bakeri to be preyed upon by the phytoseiid mite Phytoscutus acaridophagus (Collyer, 1964).

The diagnosis of Neotropacarus merely state this genus to have “certain of the body

setae long and whip like, in that certain body setae are missing” (CUNLIFFE, 1964). The

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genus, redescribe N. mumai and N. bakeri and describe three new species of belonging to this genus.

b. Material and Methods

The paratypes of N. bakeri examined in this study and types of two of the new species here described (Neotropacarus n. sp. 2 and Neotropacarus n. sp. 3) were obtained from the mite collection of the University of Michigan Museum of Zoology, Ann Arbor, Michigan, USA; the paratypes of N. mumai were obtained from the National Museum of Natural History, Washington, DC, USA. The types of Neotropacarus n. sp. 1 were collected in northeastern Brazil, whereas the other two new species (Neotropacarus n. sp. 2 and Neotropacarus n. sp. 3) were collected in the Phillipines.

Examination, measurements and illustrations were done using a microscope (Nikon Eclipse 80i); to prepare the illustrations, mites were initially photographed with a digital camera connected to the microscope, and the photos were then processed with a digital tablet (Wacom Bamboo CTH-470L), using the Adobe Illustrator® program. For the descriptions and the redescriptions, average measurements in micrometers are followed (in parenthesis) by the minimum and the maximum; when only two specimens were examined, averages were not given. Idiosomal chaetotaxy follows the system developed by Grandjean (1939) and applied to the Astigmatina by Griffiths (1990). Leg setation follows that proposed by OConnor (2009).

c. Results

Systematics

Neotropacarus Baker

Tropacarus Cunliffe, 1964: 181; name preoccupied in Tropacarus (Acari: Oribatida) Ewing, 1917: 111.

Neotropacarus Baker, 1985: 289; Klimov, 2000: 28. Type species: Tropacarus mumai Cunliffe, 1964.

Description ofadults. Gnathosoma short and massive, not more than 1.5 times as long as wide.

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and ex always present; le present or absent, when present short); vi inserted at anterior edge of sclerite. Hysterosomal chaetotaxy complete; at least setae ex (sce), cp, e2, h1 and h2 very long; e1 either short (shorter than the distance between its basis and the posterior edge of idiosoma) or very long (extending beyond posterior edge of the body); other hysterosomal setae short. All setae setiform and smooth. Oopore and aedeagus between legs III and IV, variously shaped; oopore longer than wide. Anal opening near posterior end of the body; anal region with one, two or three pairs of paraproctal setae (setae p1 and p2 present or absent and p3 always present) and males without paranal suckers. Tarsi elongate, more than twice as long as tibiae; genu I with only one solenidion; tibiae I-II with or without c”; tarsus I with or without and tarsus II without a” (aa) and ft’ (ba); seta tc’ present or absent on tarsi I-IV; ɷ2 inserted posteriad of

ɷ1; setae a’ and pv” acute or as thin spines; tc”, p’, p”, u’, u” and s short, spine-shaped. Male tarsal copulatory suckers medial, with rod-shaped bases and wider, flat discs.

Neotropacarus mumai (Cunliffe). (Figs.1 – 6)

Tropacarus mumai Cunliffe, 1964: 181. Neotropacarus mumai. Baker, 1985: 289.

Material examined

Three paratype females and two paratype males from the Democratic Republic of Congo (mentioned as Congo): Kinshasa, on unidentified tree, 16.iv.1955, E.W. Baker coll., deposited at National Museum of Natural History, Washington, DC, USA.

Diagnosis

Females and males with dorsal seta le present, seta e1 shorter than the distance between its basis and the posterior edge of idiossoma; anal region with three pairs of proctal setae; tibiae I-II without c”; tarsus I with a" and ft'; tarsi I-II without a' e pv”

Description

Female (Figs. 1 – 3; n = 3)

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Dorsum: prodorsal sclerite 70 – 82, 85 – 88 wide at posterior margins and 70 – 74 at anterior margins; evenly punctate. Grandjean´s organ divided in terminal branchs; supracoxal seta (elc I) 38 (35 – 40). Dorsal setae lengths: ro 71 (70 – 74), le 9 (9 – 10), in 48 (38 – 56), ex 302 (265

– 350), c1 30 (27 – 32), c2 31 (28 – 36), cp 354 (325 – 412), d1 27 (23 – 30), d2 28 (24 – 34), e1 33 – 48, e2 365 (320 – 425), f2 20 – 22, h1 380 – 500, h2 315 (275 – 350) and h3 137 (112

– 162). Opisthonotal gland slightly posteriad of e1; liryfissure ia close to c1; im close to opisthonotal gland and ip close to h1.

Figure 1 - Neotropacarus mumai (Cunliffe) (female). (A) Dorsal view. (B) Ventral view.

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Figure 2 - Neotropacarus mumai (Cunliffe) (female). (A) Spermatheca. (B) Gnathosoma - a- subcapitular (subc); b- supracoxal (elcp); c- dorsal palptibial; d- lateral palptibial; e- dorsal palptarsal; f- terminal palptarsal solenidion. (C) Grandjean´s organ. (D) Chelicera.

Gnathosoma: chelicera 86; fixed and movable digits respectively 21 and 26 long. Setal lengths: cheliceral 4 (spiniform), subcapitular 26 – 35, dorsal palptibial 10, lateral palptibial 18 (18 –

19), dorsal palptarsal 13 – 14, terminal palptarsal solenidion 4 and elcp 9 long.

Legs: leg I 140 – 182, tarsus 72 (70 – 73). Setal lengths: trochanter- v’ 38 (32 – 43); femur- bv”

36 (34 – 40); genu- l’ 45 (42 – 48), l” 43 (39 – 50) , σ’ 20 (19 – 21); tibia- v’ 26 (22 – 28), Φ

100 (92 – 108); tarsus- ω1 thin and straight, 17 (15 – 19), ε as a small spine 4 (4 – 5), ω2

straight, 4 (4 – 5), a” 18 (15 – 21), ω3, straight, 13 (12 – 13), ft’ 21 (18 – 25), pv’ 37 (34 – 42),

ft” 31 (27 – 35), tc” 6, p’ 8 (8 – 9), p” 9, u’ 5, u” 5 (5 – 6) and s 4 (4 – 5).

Leg II 167 (160 – 175), tarsus 76 (73 – 78). Setal lengths: trochanter- v’ 29 (24 – 32); femur-

bv” 44 (38 – 50) ; genu- l’ 33 (32 – 34), l” 34 (32 – 35), σ’ 17 (15 – 18); tibia- v’ 27 (25 – 29),

Φ 98 (90 – 106); tarsus- ω1 17 (14 – 19), pv’ 35 (32 – 39), ft” 33 (31 – 35), tc” 5 (4 – 5), p’ 7 (7 – 8), p” 7, u’ 6 (5 – 6), u” 6 (5 – 6) and s 5.

Leg III 175 (170 – 180), tarsus 77 (76 – 78). Setal lengths: trochanter- v’ 33 (30 – 35); genu- l’ 37 (34 – 42), σ’ 9 (7 – 10); tibia- v’ 42 (39 – 45), Φ 105 (95 – 112); tarsus- ft” 39 (33 – 45), tc” 6, p’ 6 (6 – 8), p” 6 (6 – 7), u’ 5 (5 – 6), u” 5 and s 5.

Leg IV 148 – 188, tarsus 85 (80 – 90). Setal lengths: femur- bv” 32 – 35; tibia- v’ 34 (32 – 38),

Φ 56 (50 – 64); tarsus- pv’ 10 (9 – 10), pv” 39 (32 – 50), ft” 36 (32 – 41), tc’ 5 (4 – 6), p’ 5, p”

5 (5 – 6), u’ 4, u” 5 and s 4.

Male (Figures 4 – 6; n = 2).

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Figure 3 -Neotropacarus mumai (Cunliffe) (female). (A) Leg I. (B) Tarsus I- dorsal view. (C) Tarsus I- ventral view. (D) Leg II. (E) Tarsus II- dorsal view. (F) Tarsus II- ventral view. (G) Leg III. (H) Tarsus III- dorsal view. (I) Tarsus III- ventral view. (J) Leg IV. (K) Tarsus IV- dorsal view. (L) Tarsus IV- ventral view.

Dorsum: prodorsal sclerite 55 – 58, 45 – 48 wide at anterior margin and 64 – 68 wide at posterior margin. Supracoxal seta (elc I) 25 – 26. Setal lengths: ro 48 – 55, le 4 – 5, in 24 – 30, ex 200 – 225, c1 14, c2 18 – 21, cp 180 – 185, d1 17 – 20, d2 15 – 18, e1 28 – 29, e2 175 – 180, f2 12 – 13, h1 212 – 250, h2 157 – 170 and h3 85 – 90. Opisthonotal gland about in transverse line with e1.

Venter: setal lengths: c3 22 – 24, 1a 18 – 20, 3a 18 – 20, 4a 20 – 22, 4b 16 – 17, g 20 – 23, p1 10, p2 11 and p3 5 – 6. Aedeagus curved at the tip, 12.

Gnathosoma: chelicera 74; fixed and movable cheliceral digits 16 and 23. Setal lengths: cheliceral 3, subcapitular 15, dorsal palptibial 8, lateral palptibial 14, dorsal palptarsal 12, terminal palptarsal solenidion 4 and elcp 4.

Legs: leg I 137, tarsus 53. Setal lengths: trochanter- v’ 20 – 22; femur- bv” 21 – 29; genu- l’ 23

– 28, l” 19 – 20, σ’ 14 – 15; tibia- v’ 13 – 14, Φ 75 – 78; tarsus- ω1 12 – 14, ε 3, ω2 3 – 4, a”

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Figure 4 - Neotropacarus mumai (Cunliffe) (male). (A) Dorsal view. (B) Ventral view.

Leg II 125, tarsus 55. Setal lengths: trochanter- v’ 19 – 20; femur- bv” 25 – 28; genu- l’ 23 – 25, l” 19 – 20, σ’ 13 – 14; tibia- v’ 14, Φ 74 – 80; tarsus- ω1 13 – 14, pv” 22 – 24, ft” 21 – 25,

tc” 4, p’ 4 – 5, p” 4, u’ 3 – 4, u” 4 and s 3.

Leg III 142, tarsus 54. Setal lengths: trochanter- v’ 18 – 20; genu- l’ 16, σ’ 6 – 7; tibia- v’ 22 – 28, Φ 65 – 70; tarsus- ft26 – 30, tc” 4 – 5, p’ 4, p” 4, u’ 3, u” 3 and s 3 (3 – 4).

Leg IV 125, tarsus 54. Setal lengths: femur- bv” 18 – 19; tibia- v’ 21 – 23, Φ 24 – 29; tarsus

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Figure 5 -Neotropacarus mumai (Cunliffe) (male). (A) Aedeagus.

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